RESEARCH ARTICLE

Site conditions for regeneration of climax

species the key for restoring moist deciduous

tropical forest in Southern Vietnam

Ha T T DoID12 John C Grant1 Heidi C Zimmer1 Bon N Trinh2 J Doland Nichols1

1 Forest Research Centre Southern Cross University Australia 2 Silviculture Research Institute Vietnam

Academy of Forest Sciences Ha Noi Vietnam

tdo16studentscueduau

Abstract

Understanding the requirements and tolerances of the seedlings of climax species is funda-

mental for tropical forest restoration This study investigates how the presence and abun-

dance of seedlings of a previously dominant now threatened species (Dipterocapus dyeri

Pierre) varies across a range of environmental conditions Dipterocapus dyeri seedling

abundance and site characteristics were recorded at 122 observation points (4 m2) at nine

clusters from two sites Seedling presence (p = 0065) and abundance varied significantly (p

= 0001) between the two sites and was strongly correlated with adult D dyeri dominance

and lower soil pH and weakly correlated with canopy openness and total stand basal area

Dipterocarpus dyeri seedlings were also grown in shade houses with three light levels on

two soils Seedling survival was significantly lower at the lowest light level (lt10 full irradi-

ance) at 13 for the forest soil and 25 for degraded soil At higher irradiance the seedling

survival rates were greater than 99 Moisture levels remained high at the lowest light level

and many seedlings died from fungal infection We concluded that secondary forests which

contain adequate numbers of adult D dyeri as seed sources light availability soil pH of lt50 and good drainage strongly favour survival and growth of D dyeri seedlings Histori-

cally D dyeri was dominant in moist deciduous tropical forest across south-eastern Viet-

nam but today it is rare Active management of these recovering forests is essential in order

to recover this high-value climax forest species

1 Introduction

Water nutrients and light are key elements in plant growth and survival These resources vary

spatially often with topographic gradients and temporally including as they interact with veg-

etation development Water and nutrient availability in the soil is largely driven by landscape-

scale factors such as topography substrate and climate [12] Light availability on the forest

floor is largely determined by the density of the forest canopy (ie local-scale factors) which

changes through time as the forest develops [34] Competition for light is a major influence

on recruitment in old-growth tropical forest [5] However in secondary tropical forest

PLOS ONE

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OPEN ACCESS

Citation Do HTT Grant JC Zimmer HC Trinh BN

Nichols JD (2020) Site conditions for regeneration

of climax species the key for restoring moist

deciduous tropical forest in Southern Vietnam

PLoS ONE 15(5) e0233524 httpsdoiorg

101371journalpone0233524

Editor Arun Jyoti Nath Assam University INDIA

Received December 19 2019

Accepted May 6 2020

Published May 29 2020

Peer Review History PLOS recognizes the

benefits of transparency in the peer review

process therefore we enable the publication of

all of the content of peer review and author

responses alongside final published articles The

editorial history of this article is available here

httpsdoiorg101371journalpone0233524

Copyright copy 2020 Do et al This is an open access

article distributed under the terms of the Creative

Commons Attribution License which permits

unrestricted use distribution and reproduction in

any medium provided the original author and

source are credited

Data Availability Statement All relevant data are

within the paper and its Supporting Information

files

Funding This study was undertaken as part of

HDrsquos PhD research program HDrsquos PhD is

competition for water is more important than competition for light and drought tolerance is

critical for survival [6ndash8] This is because there is often more light reaching the forest floor

due to gaps in the canopy Gap size directly influences light availability at the soil surface

which not only affects the germination and growth of plants in the understory but also leads

to changes in underground processes potentially influencing soil temperature water and tree

root competition [9]ndashhigher light and temperature at the soil surface increasing the likelihood

of drought [10] For example single tree fall gaps can expose high-nutrient soil ideal for germi-

nation [1112]

The mosaic distribution patterns of tree populations and tree ages in tropical forests are the

results of species-specific and tree age-specific adaptations to the spatial distributions of water

and nutrients [13ndash16] Soil type topography and vegetation structure interact to influence

seedling establishment spatially and temporally [17ndash19] The structure and composition of a

vegetation community are maintained temporally by speciesrsquo successful regeneration [11] Dif-

ferent species have different environmental requirements and different levels of tolerance to

the stresses presented by different environmentssite-conditions For example low soil pH is

tolerated by many conifer species [20] The optimum range for growing most pine seedlings is

around 45 to 50 for sandy soils and 50 to 55 for fine-texture soils containing high levels of

Mn [21] Wollemia nobilis seedlings for example have an optimum soil pH of around 43 [22]

Wollemia nobilis like many other conifers thrives at light levels higher than typically occurs in

most rainforest understories In contrast many broadleaf tropical species seedlings such as

Neolitsea obtusifolia Hopea odorata and Brosimum alicastrum survive better under conditions

those low light levels [23ndash26] In order for recruitment to be successful seeds need to fall

where light and soil moisture conditions are favourable for germination and growth [627] In

some cases the original conditions that have led to occupation by a specific vegetation may

change to be no longer suitable for its regeneration The regeneration of a species in tropical

forest can therefore be discontinuous with not all life stages of all species present Mimicking

these natural processes close-to-natural silviculture techniques and nurse crop establishment

were used commonly in the tropical areas as the foundational practise for middle- or late-suc-

cessional afforestation during their seedling and sapling periods Then light liberation is

applied as seedling increase in height depending on specific species light requirements [28ndash

31]

The key to regeneration may be related to the availability of appropriate microsites ie

small-scale variation in resources and species-specific effects [3233] When forest stand struc-

ture influences the distribution of water nutrient and light at the local scales the species com-

position showed local ecological intra and inter species effects provided a strong influence on

seedling growth [32] Conspecific density (also known as congeneric) affects not only seed

availability [34ndash36] but also physically and biologically affects seed germination survival and

growth of seedlings through negative-density dependence mechanisms [37ndash39] Negative-den-

sity dependence mechanisms were shown to strongly negatively influence same species in

monoculture plantation [374041] In mixed species natural forests negative-density depen-

dence trends (from positive to negative) with strength of the negative-density dependence

mechanism on specific-species recruitment strongly depended on the quality and quantity of

adult trees in the site (ie density distribution and size of remnant trees)

Dipterocarpaceae was previously abundant throughout southeast Asia however most

remaining forests are heavily disturbed and are dominated by deciduous tree species and bam-

boo [42ndash44] Dipterocarp species are known to be strongly associated with specific soil and

light conditions especially as seedlings Microsite light availability determined by gap size is

likely to be the most influential factor in natural regeneration of dipterocarps as dipterocarp

speciesrsquo light requirements change with life stage They prefer shade for germination partial

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supported by Vietnam Government Ministry of

Education and Training lsquoVietnam International

Education Development Programrsquo scholarship

(subsidence living expenses) SCU Forest Research

Centre has provided a scholarship for HDrsquos

university fees HDrsquos research occurred within the

broader projectĐTĐLXH1015 which is funded

by the Vietnam Government Ministry of Science

and Technology at DNBR The funders had no role

in study design data collection and analysis

decision to publish or preparation of the

manuscript

Competing interests The authors have declared

that no competing interests exist

light during seedling and sapling stages and full light as mature trees [45ndash47] The effect of

light availability appears to be stronger than the effect of foliar herbivory on Dipterocarp seed-

ling survival and growth [4849] Understanding patterns of natural regeneration of diptero-

carps will contribute to efforts to restore and re-establish this highly valued and important

type of forest [50ndash52]

Dipterocarpus dyeri is native to Myanmar Thailand Viet Nam Cambodia and Peninsular

Malaysia The species has been globally assessed as Endangered in the IUCN Red list [5354]

Most dipterocarp species including Dipterocarpus dyeri Pierre are high value timber species

and as such have been selectively logged across South-east Asia [42] Dipterocarpus dyeri has

been targeted in particular because of its high density wood (~ 08 gcm3) and also their resins

(dammar) which can be extracted for caulking boats varnish paint and medicine [4254ndash57]

Dipterocarpus dyeri today is one of the rarest species in the forest and there is limited informa-

tion on species ecology regeneration and growing site conditions [5458]

Seedling recruitment is a crucial process in long term forest dynamics An accurate under-

standing of tree recruitment patterns in forest stands and microhabitats is required to predict

forest development and optimise forest management to achieve ecological andor production

goals [59ndash61] This study aimed to determine the primary ecological processes driving Diptero-carpus dyeri seedling establishment and survival The micro-scale conditions belong to three

main groups (1) soil including particle size distribution and chemical properties and encom-

passed in soil type (2) site including topographic wetness and (3) forest stand characteristics

including canopy openness basal area species biodiversity and dominance of adult D dyeriDetermining the requirements for D dyeri seedlings will improve understanding of secondary

forest regeneration This will help land managers to choose suitable sites to manage regenera-

tion prepare and plant nursery stock and develop appropriate silviculture techniques for res-

toration of dipterocarp forests in southeast Vietnam

2 Methods

21 Study sites

The study was conducted in a monsoonal evergreen broad-leaved forest in the Dong Nai Bio-

sphere Reserve (DNBR) Dong Nai Province Vietnam (Fig 1 the maps were sourced from

Natural Earth [62]) which are licensed under a CC BY-SA 40) The Director of DNBR Dr

Tran Van Mui gave permission to conduct this research project in DNBR The Reserve

extends between 11˚20rsquo50rdquoNndash 11˚50rsquo20rdquoN and 107˚09rsquo05rdquoEndash 107˚35rsquo20rdquoE [63] The area is in

the lowland monsoon tropical climate zone with mean annual rainfall of 1850 mm of which

80 falls in the wet season (from April to October) The mean annual temperature is approxi-

mately 26˚C with small seasonal fluctuations [64]

Two study sites were established with elevations that ranged from 44 to 130 m asl A mixed-

bamboo (MB) site (UTM 48N 736532E 1257916N (Plot SK3)gt 100 m elevation) at Phu Ly

Commune was in a steep landscape (10-20˚) and a mixed-evergreen (ME) site (UTM 48N

716275E 1236117N (Plot DD2) 70ndash95 m elevation) occurred on gentle slopes

The soils at both sites were classified as Acrisols (grey podzolic soils) [65] The ME site soils

are mapped as Chromic Acrisols (Fp) developed on old alluvium These soils are yellowish

brown and clayey throughout with a Bts horizon at 30ndash100 cm depth The MB site soils are

Endolithic Chromic Acrisols (Fs) which had developed on schist and shales [65] The soils in

this site are shallow (50ndash70 cm) yellowish brown sandy clay loam to light clay textures and a

BCts horizon at 30ndash40 cm above R or C horizons The soil chemical analysis (S1 Table) showed

a high level of base saturation (more than 50) indicating both soils might be better classified

as Luvisols [66]

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The forests in the study area are lowland tropical forests dominated by dipterocarp and

Lagerstroemia (Lythraceae) species [67ndash69] Most of forests in the area are recovered after log-

ging (early 1943 and from 1976 to 1996) herbicide spraying (1961ndash1971) and other deforesta-

tion activities (1976ndash1996) [7071] The forests at the ME site contained mixed evergreen tree

species (D dyeri Hopea recopei Vatica odorata Artocarpus spp Syzygium spp) and decid-

uous species (Lagerstroemia spp Cratoxylum spp Nephelium melliferum) The MB site was

dominated by bamboos which were considered as a regrowth stage of broadleaf forest after dis-

turbances [6869]

22 Study species

Dipterocarpus dyeri is a large lowland evergreen rainforest tree species It also occurs in dry

evergreen forests as a brevideciduous species as they lose their leaves for only a few days

[4272] In DNBR according to our observations since 2016 fruiting of adult D dyeri trees

(DBH more than 40 cm) occurs almost every year with flowering in NovemberndashDecember

and fruit maturation in MarchndashApril

Fig 1 Location of study site and plots in Dong Nai Province Vietnam Colours on the basemap represent forested (green) and unforested (yellow

and brown) land cover The land cover basemap country and province borders were sourced from NaturalEarth (httpwwwnaturalearthdatacom

aboutterms-of-use)

httpsdoiorg101371journalpone0233524g001

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23 Data collection

The data from the forests were collected during the dry season in November 2017 ndashJanuary

2018 inside the DNBR (Fig 1) A total of 122 observation points (2 m x 2 m) were taken from

18 sampling clusters (represented by plot vegetation data Table 1 Fig 1 S1 Data) The loca-

tions of these clusters and points were allocated on two sites with 101 points (15 plots) on

Mixed Evergreen (ME) and 21 points (3 clusters) on Mixed Bamboo (MB) approximately 20

km from ME site (Fig 1) First we identified potential D dyeri (DBH gt 40 cm) mother trees

Then a search for D dyeri seedlings was undertaken with distance from the mother tree 100

m If a seedling was found then that seedling became a corner of a 400 m2 plot Then all seed-

lings within that area were identified and measured If no seedlings were found then a similar

400 m2 plot was established for surveying site and soil conditions with a mother tree as the

centre and five observation points (each of the four corners and at the centre of the plot)

231 Vegetation composition In each plot all woody species (excluding lianas) were

recorded and divided into three classes based on the diameter at 13 m height from the ground

(DBH) adults (DBH 10 cm) juveniles (5 cm DBH lt 10 cm) Adults and juveniles were

surveyed from 400 m2 plots while seedlings of all species were surveyed from the observation

points

232 Soil At each observation point a description of soil from 0ndash35 cm depth was made

including horizons colour and texture One topsoil (0ndash10 cm depth) sample which was a mix-

ture of soil from 3ndash5 observation points was taken for soil chemical characterisation of each

Table 1 Description of soil and site characteristics from 122 observation points

Variable Abbreviation Mixed Evergreen Mixed Bamboo

Cluster Plot 15 3

Observation points (presence) 101 (67) 21 (9)

Elevation (m) Elevation 83 (13) 137 (26)a

Parent materials Parentm Alluvium Schist and Shale

Slope (Degrees) Slope 86 (74) 117 (75)a

Stand basal area (m2Ha) BA 353 (126)a 175 (166)

Dominance of adult D dyeri PDA 027 (018)a 022 (008)

Count of D dyeri seedlings dyeri 11 (16)a 04 (05)

Canopy openness () CO 129 (35) 163 (51)a

Topographic Wetness Index TWI 111 (203) 103 (133)

Topsoil bulk density (gcm3) TopsoilBD 113 (021) 111 (004)

Topsoil pH (KCl) pH 38 (02) 37 (01)

Topsoil organic carbon () OC 26 (11) 197 (02)

Topsoil total nitrogen () N 023 (006) 021 (002)

Carbon Nitrogen ratio CN 107 (198)a 93 (03)

Total phosphorous (mg100g) P2O5 76 (28)a 52 (015)

Cation Exchange Capacity CEC 85 (26) 89 (09)

Sand (02ndash2 mm) () Sand 24 (12)a 17 (8)

Fine Sand (005ndash02 mm) FineSand 18 (6) 20 (7)a

Silt (0002ndash005 mm) Silt 30 (12) 31 (7)

Clay (lt0002 mm) () Clay 26 (13) 32 (6)a

Fine particles Silt + Clay () Siltclay 57 (14) 63 (4)

Mean (SE)a Significant different between two site with wilcoxtest function significant level 005 [79]

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sampling cluster At each sampling cluster one core sample (5 cm diameter x 5 cm length) was

taken for topsoil bulk density calculation

233 Light A hemispherical canopy photograph was taken at each observation point at

170 cm above the ground We chose this height to avoid the shrub and herb layers These pho-

tos were used to determine canopy openness () using Gap Light Analyzer (GLA) software

[73] after processing the image through SideLook [74] using automatic thresholding The pro-

cedure of using automatic threshold to adjudge colour canopy photographs is recommended

for assessing canopy openness [75]

234 Environment Basic site conditions were described at each observation point

including slope (degrees) aspect (degrees) outcrop rock ( cover) forest floor vegetation

cover () litter cover () and litter thickness (cm) Topographic wetness index (TWI) [76]

was calculated as a soil moisture indicator [7778] for each observation point was derived by

Arctoolbox from a digital elevation model (DEM) through SAGAGIS AcrGIS v 101 A DEM

of 30 x 30 m grid spacing was downloaded from httpsearthexplorerusgsgov

235 Shade house experiment establishment Seeds were collected from one mother tree

from Cay Gui Forest Ranger Station (approximately 500 m from plot CG1) The seedlings

were germinated using moist sand for 20ndash30 days until developing to seedlings with two true

leaves (S2A Fig) which were then transplanted in plastic pots (8 cm diameter x 40 cm height)

There were six treatments of three light levels (high medium and low) and two sources of soil

(old growth forest and heavily logged and degraded forest) with a total of 432 seedlings (72

seedlings per treatment) Each light treatment was set up in a shelter with light levels controlled

by shade cloth one layer for the high level doubling for the medium level and tripling for the

low level The light levels were confirmed by the measurement of leaf area index (LAI) by

using Li-2200 The LAI at the three shelters were 29 54 and 71 giving estimations of canopy

openness for each light levels were proximately 45 20 and 5 of full sun respectively Soil

used for the trial was the topsoil of a Chromic Acrisol (Fp) and it was collected from two sites

Both soils were light clays in texture and the old growth forest soil (F) was higher in organic

matter total nitrogen and CEC than the degraded site soil (D) (S1 Table)

24 Data analysis

241 Forest data Correlation between presencenumber of D dyeri seedlings and

microsite conditions The effect of site (mixed evergreen and mixed bamboo sites) on the

assemblage of seedlings of the target species per observation point was tested using multivari-

ate models [80] through manyglm function in mvabund R package [81] This function analyses

the individual and interactive influences of each site condition variable based on mixed effect

models Negative binomial family of distribution link was chosen as seedling abundance data

was overdispersed

The sets of variables were also used to test their effects on presence and abundance of D

dyeri seedlings at observation points in generalized linear regression models (GLM) We used

the glmnb function within lsquoMASSrsquo [82] to fit models with a negative binomial family with dis-

tribution for data collected at observation points where seedlings occurred We also used func-

tion glm from package lsquolme4rsquo [83] with binomial family for presenceabsence data In the

GLM the cluster (plot) of observation point was not treated as random factor since the forest

stand variables were aggregated in the cluster The final models were selected by AIC in the

stepwise search through function step in stats R package stats [79]

As canopy openness was one of the factors of most interest in the forests we used Bayes t

test function in BayesianFirstAid R package [84] to compare the difference in canopy openness

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against seedling abundance level groups and between presence and absence groups for all

observation points and for each site

242 D dyeri seedling in shade houses Influence of soil and light To investigate the

differences in seedling survival according to light level and soil we used the Pearson Chi-

squared test Analysis of variance (ANOVA) was used to compare the differences in seedling

growth (based on diameter and height) among treatments (soil types and light levels and their

interactions)

3 Results

31 Forest data Differences in seedling abundance in varying soil and site

conditions

Correlations between soil and stand properties differed between the two sites (S1 Fig) Stand

basal area (BA) was weakly correlated with canopy openness (CO) on the mixed evergreen

(ME) site and moderately correlated with proportion of adult D dyeri on the higher elevation

mixed bamboo (MB) site Canopy openness showed weak negative correlations with soil CN

P2O5 and sand content and these correlations were similar on the higher site (S1 Fig) For the

observation points where the seedlings were present the correlations of site and soil properties

were quite similar to the correlations at all observation points (S1 Fig)

The multivariate test of deviance indicated a significant effect of site on D dyeri seedling

abundance (p = 0001) and no significant effect on D dyeri presence (p = 0065) Both the

abundance and presence of D dyeri seedlings were positively correlated with the site ME asso-

ciation with coefficients (Wald value) of 25 and 198 respectively

Seedlings were more likely to be present in darker sites (Table 2 Fig 2 S1 Fig) The associa-

tion of D dyeri seedling with lower CO was also indicated by the mean difference in CO

Table 2 Results for four generalized linear models which predict presence and abundance of D dyeri seedlings per observation point at both sites (models 1 and 2)

and at the mixed evergreen (models 3 and 4) site only ME Mixed evergreen MB Mixed bamboo BA Stand basal area PDA Dominance of adult D dyeri

Model Parameter Estimate StdDev Std Error p AIC Deviance explain by the model

(1) Presence of seedlings Intercept 3653 1107 0001 1536 112

BA -0028 0016 0069

PDA 4358 1584 0006

openness -0171 0054 0001

Silt -0035 002 0084

(2) Abundance of seedlings Intercept 533 2109 00115 2277 2884

BA 0025 0007 00004 Std Err 258

pH -152 057 0008 Theta 196

(3) Presence of seedling on ME site Intercept 5978 1498 0000 1131 353

BA -0083 0025 0001

pH -1817 1227 0138

PDA 7781 2244 00005

openness -0207 0077 0007

Silt -007 0027 001

(4) Abundance of seedlings on ME site Intercept 4597 2359 00514 2916 84

PDA 0029 001 00295 Std Err 092

pH -1302 06323 00395 Theta 232

(5) Presence of seedlings on MB site Intercept -93448 69728 018 32384 80

Silt 0301 0225 0181

pH 22747 17083 0183

httpsdoiorg101371journalpone0233524t002

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between the presence and absence observation points of -21 (95 credible interval from -36

to -065) (Fig 2A) The lower CO was also found on ME site with the mean difference of CO

between presence and absence points was -19 (95 credible interval from -33 to -048) (Fig

2B) However the lower CO points where D dyeri seedlings were absent on the MB site was

not clear with mean of difference with the present points was -11 (95 credible interval from

-64 to 41) (Fig 2C) The results of the GLM also indicated that presence of seedlings signifi-

cantly negatively correlated with CO on both sites (p = 001) and with ME site (p = 0007) but

not correlated with the MB site (Table 2)

The dominance of adult D dyeri trees (PDA) was positively correlated with the presence of

seedlings for both sites (p = 0006) PDA was positively correlated with presence and abun-

dance of seedling on ME site but was not correlated to these variables on the MB site

(Table 2) The results from BMA showed that PDA was the fourth most important variable in

the presence of seedling model with a probability of 46 coefficient is not equal to zero coeffi-

cient of 1704 (plusmn 2218) but PDA was the least important variable in the abundance model

with only 74 probability that coefficient is not equal to zero coefficient of -0018 (plusmn 0176)

Seedling abundance was not correlated with CO (Table 2) but it was marginally negatively

correlated with stand total basal area (BA) with p = 0069 (Table 2 but when seedlings were

present their abundance was positively correlated with stand total basal area (p = 00004

Table 2) The correlations of BA with seedling presence and abundance were significant on the

ME site with a negative correlation with presence and positive correlation with abundance

However all of the variables included in the model-averaged analysis were not always nega-

tively or positively correlated with abundance of seedlings (S2 Table) Comparing with other

factors BA showed weaker effects to seedling presence than CO and weaker effects than soil

pH to the seedling abundance (Table 2)

When analysed across both sites seedling abundance was negatively correlated with soil pH

and positively correlated with BA (Table 2) In contrast when the data for the ME site was ana-

lysed separately there was a significant negative correlation between abundance and PDA

(p = 003) and also with soil pH (p = 004) (Table 2) This consistent negative correlation of pH

with abundance of seedlings is reflected in a probability of 95 coefficient of pH not equal to

zero out of 97 all the BMA models with coefficient of -1619 (plusmn 0629) (S2 Table) In the set

Fig 2 Difference of means of canopy openness () between presence (μ1) and absence (μ2) of seedlings for all data (A) for points on mixed

evergreen site (B) and for points on bamboo dominant site (C)

httpsdoiorg101371journalpone0233524g002

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of models for abundance of seedlings on both sites pH was included in less than 50 of the

models and inconsistently negatively or positively correlated with coefficient of -0529

(plusmn 0677) Overall at both sites soil pH was low (typically less than 50) (Table 1) Topsoil silt

content had a weakest negative correlation (coefficient = -007 p = 001) with seedling pres-

ence only on the ME site (Table 2)

32 Shade house study Seedlings response to light and soil treatments

After 10 months the seedlings grown in the lowest light level had significantly lower survival

rates compared with those at higher light levels (χ-squared = 8351 df = 5 plt 000) While

most of the seedlings at medium and high light levels survived (99 survival only one seedling

died in FM treatment) only 194 of seedlings at the lowest light level survived (Table 3) The

effect of soil type on seedling survival was evident at the lowest light level with 25 survival of

seedlings on degraded soil compared to only 14 seedling survival on forest soil (Table 3) At

the highest light level soil type also appeared to have an effect on seedling health with a lower

rate of seedlings with leaf damage (holes or marks by fungal disease or insects) on the forest

soil (167) compared to degraded soil (25)

ANOVA results showed that light level soil and light soil interaction significantly influ-

enced seedling height (p = 003 Fig 3) however only light level resulted in a significant differ-

ence in seedling diameter (p = 0000 Fig 3) The seedlings grown at a high light level grew

higher (LowndashHigh = -371 p = 0000 MediummdashHigh = -2635 p = 0000 Mediumndash

Low = 1075 p = 0001) and larger (LowndashHigh = -188 p = 0000 MediummdashHigh = -206

p = 0000 MediumndashLow = -019 p = 073) than those in low light levels (Fig 3) Soils signifi-

cantly influenced the seedling height at the high light level treatment (p = 0000 Fig 3A) The

seedlings grown on forest soil had significantly higher stem height (ForestmdashDegraded = 639

p = 0000 Fig 3A) and slightly larger diameters than those grown in degraded soil (Forestmdash

Degraded = 015 p = 029 Fig 3B) and The seedlings grown at low and medium light levels

were very similar in growth with no difference between the two soils

The data on seedling leaf characteristics after 10 months was collected from shade house

component of three light levels and two soil type Leaf morphology and anatomy were signifi-

cantly different among light and soil treatments (Fig 4) Seedlings in higher light and on forest

soil had greater leaves of leaf length (plt 0001) and leaf width (plt0001) (Fig 4A and 4B) but

thinner leaf thickness (Fig 4C) except at the medium light level leaves of seedlings on forest

soil and degraded soils were not significant in length and wide The leaves of seedlings on for-

ested soil were thinner than those on degraded soil (plt 0001) Leaf stomatal density was posi-

tively correlated with light levels and seedlings on degraded soil treatments had higher leaf

stomatal density compared to those on forest soil treatments (Fig 4D) Leaf chlorophyll

Table 3 Seedling survival and health status depending on soils and light levels

Treatment Survival Health status (leaf damage)

Seedling Rate () Seedling Rate ()

FH 72 100 12 167

DH 72 100 18 250

FM 71 986 19 264

DM 72 100 18 250

FL 10 139 10 100

DL 18 250 18 100

F Forested soil D Degraded soil H High light level M Medium light level L Low light level

httpsdoiorg101371journalpone0233524t003

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content was negatively correlated to light level (Fig 4E) Soil type had a significant effect on

chlorophyll content at both low and high light levels but not significant at the medium light

level At the low light level seedlings on forest soil had lower leaf chlorophyll content than

those on degraded soil and the opposite result was shown at high light level

4 Discussion

Dipterocarpus dyeri seedlings were more likely to be present at sites with lower canopy open-

ness (Table 1 Table 2 Fig 2) Previous studies have shown that D dyeri is a typical climax trop-

ical shade-tolerant species in Dong Nai [4258] and this is supported by our results In our

study the seedlings that survived in low light level conditions had higher leaf chlorophyll con-

tent and stomata density (Fig 4) indicating that D dyeri has high light capture efficiency at low

light availability [85] In addition D dyeri is a large-seeded species (S2B Fig) with recalcitrant

seeds [54] a further indicator that it is a shade tolerant tropical climax species [86] Seedlings

which have high leaf area such as D dyeri are more likely disadvantaged in large gaps because

of dryer soil higher temperature and greater water loss through their leaves [87] The D dyeriseedlings growing in the forest understory tended to have a lateral branching trait (S2C Fig)

which allows maximum light capture in shade [88] Our finding that D dyeri seedlings

occurred in sites with low light is consistent with previous research that concluded that the

late-successional tropical seedlings in the Dipterocarpus genus are the most shade-tolerant

genus in the Dipterocarpaceae family [4289ndash91]

Fig 3 Seedlings growth in base diameter (A) and height (B)

httpsdoiorg101371journalpone0233524g003

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 10 20

Fig 4 Influence of soils and light levels to leaves length (A) leaves wide (B) blade thickness (C) chlorophyll

concentration (D) and stomatal density (E)

httpsdoiorg101371journalpone0233524g004

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 11 20

Dipterocarpus dyeri appears to be a broadly adapted generalist dipterocarp species that can

survive and grow in a broad range of light and soil conditions The negative correlation

between seedling presence and light was at odds with species abundance findings (which indi-

cated a positive association between abundance and light) (Table 2) This result may be due to

the limited range of light availability levels at our study sites (95 to 22) These levels fall

within the range appropriate for many shade-tolerant dipterocarps [92ndash94] In the shade

house survival and growth of D dyeri was higher at the higher light levels with only 25 of

seedlings surviving at the lowest light level (5) (Table 3) These results suggest that D dyeriprobably can persist at canopy openness lower than 10 and that it is a generalist species

rather than a shade-tolerant specialist This is consistent with the findings of Denslow [11] and

Paoli et al [94] who found that in rainforest most canopy species are neither open environ-

ment pioneer species nor shade-preferring ldquoclimaxrdquo forest species but generalists that can tol-

erate low light but require more open condition to grow into canopy trees [95ndash97]

Dipterocarpus dyeri seedling presence had a weak negative correlation with total forest basal

area (BA) (Table 2) However at the subset of sites where the seedlings were present their

abundance was positively correlated with BA (Table 2) On the surface this results seems

counterintuitive because typically sites with higher BA are also darker However in this study

canopy openness was not correlated with BA (S1 Fig) because the sampling time was in the

dry season after deciduous species had dropped their leaves Seedlings were less likely to be

present at higher BA sites because these sites were characterised by a higher deciduous compo-

nent which was typically composed of Cratoxylum and Lagerstroemia species Cratoxylumand Lagerstroemia are strongly competitive long-lived pioneer species and D dyeri seedling

survival is likely to be lower at these sites

Seedling presence and abundance were strongly positively correlated with the dominance

of mother trees (PDA) (Table 2) This result was expected for a number of reasons Firstly the

higher PDA indicated that the site conditions were suitable for the species Secondly higher

PDA suggested a more stable seed source in the recovered forest [429899] Thirdly D dyeriis a brevideciduous species with leaf-flushing within one week (this study and [42]) It can be

grouped with evergreen species similar to two other Dipterocarpus species in Thailand [72] so

where it dominates basal area the canopy in the dry season is less open (cf deciduous forests)

and lower light availability was associated with the presence of D dyeri seedlings in our study

(Fig 2) This positive correlation between presenceabundance of seedlings and mother trees

contradicts previous research describing a negative effect of conspecific adult effects (due to

impacts of pathogens and leaf litter) on the survival of early-stage seedlings which was consid-

ered to be a partial explanation for the species richness in tropical forests [100ndash103] However

conspecific negative density effects have often been found to be a weaker factor compared to

environmental conditions [47104105] Conspecific density affects differently on different spe-

cies and at different stages of forest development [106] For example D dyeri species produces

an abundance of large seeds and large seed mass can be one of the strongest factors compensat-

ing for the conspecific negative density effect [107] In Dong Nai D dyeri had been logged

[58108] resulting in the abundance of adult D dyeri present today Hence the density of adult

D dyeri trees might not be high enough to show the negative effects

Dipterocarpus dyeri seedling abundance was negatively correlated with soil pH (Table 2)

Overall at all sites soil pH was low (pH(KCl) from 36 to 40 or pH(water) of 45 to 50) (Table 1

S2 Table) Commonly climax lowland tropical species show a high tolerance to the infertile

acidic and high aluminium concentration of tropical soils (Acrisol and Ferrasols) [20] such as

occurs in dipterocarp forests However tropical soils can be very spatially variable and while

forest soils are generally of low fertility the higher fertility soils can be found on sloping sites

where the soils are younger and have undergone less leaching [20] The negative correlation

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 12 20

between seedling abundance and pH is attributed to the higher tolerance of evergreen species

to strongly acidic soils compared with deciduous species which usually prefer higher soil pH

(from 58 to 62) [20] Evergreen species are also less tolerant of low moisture than deciduous

species as occurs in these sites during the dry season Lower pH affects the availability (or is

correlated with the availability) of a range of beneficial as well as toxic minerals (aluminium

iron manganese and phosphorus) and these are likely to be the driving factor [20] The nega-

tive correlation between seedling abundance and soil pH was in contrast with findings for D

sublamellatus in Borneo which was not associated with pH [94] However in that study the

species is considered to be a soil nutrient generalist and therefore would be expected to be

more tolerant of a wide range of conditions [94]

Seedling mortality was greatest in the lowest light level in the shade house trial (Table 3)

The results show opposite trends in natural vs simulated (shade house) conditions it is possi-

ble that factors other than light might have discernible influence on the presence or absence of

seedlings Local site temporal factors such as litter thickness soil CO2 concentration presence

of herbivores and pathogens can affect germination and process of seedling establishment In

our case there was the evidence of Fusarium wilt disease (S2D and S2E Fig) which infected

the plants in the lower light and higher humidity conditions In addition while all seedlings

were given the same amount of irrigation the soils in heavy shade appeared to stay wetter This

result was similar to the lower survival of a range of tropical species under lower light availabil-

ity reported by Augspurger et al [102] and Gaviria and Engelbrecht [109] and high mortality

for Dipterocarpus seedlings at low light levels [94110] There are other possible and related

explanations for high mortality in low light Firstly seedling photosynthesis was low and lead-

ing to seedlings being less able to resist disease and insect damage Secondly saturation of the

soils could negatively affect survival of seedlings Under the low light levels the photosynthesis

rate was low meaning that less water was lost through leaves and evaporation from soil Con-

sequently the soil which was a Chromic Acrisol with a relatively high clay content maintained

high moisture levels [65111] The FeAl-rich acidic tropical soil may have become anoxic and

therefore toxic for seedlings [112] The heaviness of this soil may also explain the higher sur-

vival rate of seedlings on the lower clay content (degraded soil) at the same light level treat-

ment (Table 3) Our survey also showed that adult D dyeri were found at higher densities on

the steep sites (cluster RR1 with 80 total basal area was made of D dyeri) where the dry sea-

sons were relatively wetter and have a shorter time for which they are waterlogged during the

rainy season [17113114] Thirdly D dyeri may be maladapted to flooding and waterlogged

soils as the species shows some morphological characteristics indicative of drought tolerance

For example D dyeri seedlings have hairy leaves and deep tap roots possibly giving them

more tolerance to droughts [115ndash117]

5 Conclusions

Regeneration of D dyeri the most dominant dipterocarp species in the region is the key for

restoring the forest landscape D dyeri appears to be a broadly adapted generalist dipterocarp

species that can survive and grow in a broad range of light and soil conditions D dyeri seed-

lings also survived better where soils had low pH and good drainagedry soils rather than wet

soils The strong correlation of D dyeri seedling presence and abundance with the dominance

of mother trees is linked to the recovering status of the forest in Dong Nai At the landscape

scale sites characterised by mixed bamboo (lower available soil water and light level [118ndash

120]) and shallow soils (on schist and shale soil parent materials) have lower presence and

abundance of D dyeri seedlings indicating that such sites are less suitable for D dyeri refores-

tation of these sites should focus on other species Microsite conditions especially topographic

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 13 20

location impact on soil water regime in seasonally dry areas like Dong Nai and this contrib-

utes to the observed distribution patterns of seedlings With regard to restoration techniques

our findings suggest that (a) nurse crops are not necessary for D dyeri establishment if the site

is moist enough but (b) nurse crops should be used at drought-prone sites (c) under the most

common tree cover conditions including intermediate recovered forest or dense plantation

light liberation will be necessary for native forest restoration (d) restoration should not be

attempted on waterlogged sites and (e) using phosphorus or lime carefully to increase soil

phosphorus (but maintaining pHlt 55) should be considered

Supporting information

S1 Data Data collection methods

(DOCX)

S2 Data Data of site and soil characteristics at each observation point

(DOCX)

S1 Table Characteristics of soil used in shade house experiment

(DOCX)

S2 Table Model-averaged coefficients for site and soil effect on D dyeri seedling presence

and abundance Values presented are means across each Bayesian model averaging model set

For each parameter p 6frac14 0 is the probability that the coefficient is not equal to zero

(DOCX)

S1 Fig Correlation of soil and site properties at both sites (A) at ME only (B) at MB only

(C) and at observation points where the seedling presented only (D) Positive correlations

are displayed in grey and negative correlations in black The size of the circle are proportional

of the correlation coefficients with the significant level 005

(DOCX)

S2 Fig Germinating seeds and seedlings when transplanted in plastic pots (A) Fruit size

(B) Branching of under-canopy seedling (C) Seedling died in shade house (D) and Fusar-

ium samples (E)

(DOCX)

Acknowledgments

The authors thank Quang-Trung Nguyen and Anh-Linh Nguyen of DNBR for their supports

of collecting data in the forest and looking after the shade house experiment

Author Contributions

Conceptualization Ha T T Do John C Grant Heidi C Zimmer J Doland Nichols

Data curation Ha T T Do

Formal analysis Ha T T Do

Funding acquisition J Doland Nichols

Investigation Ha T T Do Bon N Trinh

Methodology Ha T T Do John C Grant Heidi C Zimmer J Doland Nichols

Project administration Ha T T Do

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 14 20

Resources Bon N Trinh

Supervision John C Grant Heidi C Zimmer Bon N Trinh J Doland Nichols

Visualization Ha T T Do

Writing ndash original draft Ha T T Do John C Grant Heidi C Zimmer J Doland Nichols

Writing ndash review amp editing Ha T T Do John C Grant Heidi C Zimmer J Doland Nichols

References1 Baldeck CA Colgan MS Feret J-B Levick SR Martin RE Asner GP Landscape-scale variation in

plant community composition of an African savanna from airborne species mapping Ecol Appl 2014

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2 Clark DB Palmer MW Clark DA Edaphic factors and the landscape-scale distributions of tropical rain

forest trees Ecology 1999 80 2662ndash2675 httpsdoiorg1018900012-9658(1999)080[2662

EFATLS]20CO2

3 Terborgh J Diversity and the Tropical Rain Forest New York Scientific American Library 1992

4 Lowman MD Rinker HB editors Forest Canopies Elsevier Academic Press 2004

5 Lieberman D Demography of tropical tree seedlings a review In Swaine MD editor The ecology of

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6 Whitmore TC A review of some aspects of tropical rain forest seedling ecology with suggestions for

further enquiry In Swaine MD editor The ecology of tropical forest tree seedlings Paris UNESCO

1996 pp 3ndash30

7 Burslem DFRP Differential responses to nutrients shade and drought among tree seedlings of low-

land tropical forest in Singapore In Swaine MD editor The Ecology of Tropical Forest Tree Seed-

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8 Brienen RJW Zuidema PA Martınez-Ramos M Attaining the canopy in dry and moist tropical forests

Strong differences in tree growth trajectories reflect variation in growing conditions Oecologia 2010

163 485ndash496 httpsdoiorg101007s00442-009-1540-5 PMID 20033820

9 drsquoOliveira MVN Ribas LA Forest regeneration in artificial gaps twelve years after canopy opening in

Acre State Western Amazon For Ecol Manage 2011 261 1722ndash1731 httpsdoiorg101016j

foreco201101020

10 Dam O van Forest filled with gaps Effects of gap size on water and nutrient cycling in tropical rain for-

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11 Denslow JS Tropical rainforest gaps and tree species diversity Annu Rev Ecol Syst 1987 18 431ndash

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12 Nichols JD Wagner MR Agyeman VK Bosu P Cobbinah JR Influence of artificial gaps in tropical for-

est on survival growth and Phytolyma lata attack on Milicia excelsa For Ecol Manage 1998 110

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13 Clark DB Clark DA Rich PM Comparative analysis of microhabitat utilization by sampling of tree spe-

cies in neotropical rain forest Biotropica 1993 25 (4) 397ndash407

14 PALMIOTTO PA DAVIES SJ VOGT KA ASHTON MS VOGT DJ ASHTON PS Soil-related habitat

specialization in dipterocarp rain forest tree species in Borneo J Ecol 2004 92 609ndash623 httpsdoi

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15 Neilan W Catterall CP Kanowski J McKenna S Do frugivorous birds assist rainforest succession in

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16 Toledo M Poorter L Pentildea-Claros M Alarcon A Balcazar J Leantildeo C et al Climate is a stronger driver

of tree and forest growth rates than soil and disturbance J Ecol 2011 99 254ndash264 httpsdoiorg10

1111j1365-2745201001741x

17 Becker P Rabenold PE Idol JR Smith AP Water potential gradients for gaps and slopes in a Pana-

manian tropical moist forestrsquos dry season J Trop Ecol 1988 4 173ndash184

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DC Peet RK Veblen TT editors Plant Succession Theory and prediction London Chapman amp

Hall 1992 pp 11ndash59

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20 Binkley D Fisher R Ecology and Management of Forest Soils 4th ed Hoboken NJ Wiley-Black-

well 2013

21 South DB Optimum pH for Growing Pine Seedlings Tree Plant Notes 2017 60 49ndash62

22 Offord CA Meagher PF Zimmer HC Growing up or growing out How soil pH and light affect seedling

growth of a relictual rainforest tree AoB Plants 2014 6 1ndash9 httpsdoiorg101093aobplaplu011

PMID 24790132

23 Lee DW Oberbauer SF Krishnapilay B Mansor M Mohamad H Yap SK Effects of irradiance and

spectral quality on seedling development of two Southeast Asian Hopea species Oecologia 1997

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24 Rozendaal DMA Hurtado VH Poorter L Plasticity in leaf traits of 38 tropical tree species in response

to light relationships with light demand and adult stature Funct Ecol 2006 20 207ndash216 httpsdoi

org101111j1365-2435200601105x

25 Rozendaal DMA Zuidema PA Dendroecology in the tropics A review TreesmdashStruct Funct 2011

25 3ndash16 httpsdoiorg101007s00468-010-0480-3

26 Sakai A Visaratana T Vacharangkura T Thai-Ngam R Nakamura S Growth performance of four dip-

terocarp species planted in a Leucaena leucocephala plantation and in an open site on degraded land

under a tropical monsoon climate Japan Agric Res Q 2014 48 95ndash104 httpsdoiorg106090jarq

4895

27 Bowman DJMS Panton WJ Factors that control monsoon-rainforest seedling establishment and

growth in North Australian J Ecol 1993 81 559ndash567

28 Holl KD Zahawi RA Cole RJ Ostertag R Cordell S Planting Seedlings in Tree Islands Versus Planta-

tions as a Large-Scale Tropical Forest Restoration Strategy Restor Ecol 2011 19 470ndash479 https

doiorg101111j1526-100X201000674x

29 Dong TL Forrester DI Beadle C Doyle R Hoang NH Giap NX et al Effects of light availability on

crown structure biomass production light absorption and light-use efficiency of Hopea odorata

planted within gaps in Acacia hybrid plantations Plant Ecol Divers 2017 9 1ndash14 httpsdoiorg10

10801755087420161262471

30 Cole RJ Holl KD Keene CL Zahawi RA Direct seeding of late-successional trees to restore tropical

montane forest For Ecol Manage 2011 261 1590ndash1597 httpsdoiorg101016jforeco201006

038

31 Dong TL Beadle CL Doyle R Worledge D Site conditions for regeneration of Hopea odorata in natu-

ral evergreen dipterocarp forest in Southern Vietnam J Trop For Sci 2014 26 532ndash542

32 Mayoral C Van Breugel M Turner BL Asner GP Vaughn NR Hall JS Effect of microsite quality and

species composition on tree growth A semi- empirical modeling approach For Ecol Manage 2019

432 534ndash545 httpsdoiorg101016jforeco201809047

33 Salinas-Peba L Parra-Tabla V Campo J Munguıa-Rosas MA Survival and growth of dominant tree

seedlings in seasonally tropical dry forests of Yucatan Site and fertilization effects J Plant Ecol 2014

7 470ndash479 httpsdoiorg101093jpertt055

34 Maycock CR Thewlis RN Ghazoul J Nilus R Burslem DFRP Reproduction of dipterocarps during

low intensity masting events in a Bornean rain forest J Veg Sci 2005 16 635ndash646 httpsdoiorg10

1111j1654-11032005tb02406x

35 Seidler TG Plotkin JB Seed dispersal and spatial pattern in tropical trees Nathan R editor PLoS

Biol 2006 4 0001ndash0006 httpsdoiorg101371journalpbio0040344 PMID 17048988

36 Lutz JA Larson AJ Swanson ME Freund JA Ecological importance of large-diameter trees in a tem-

perate mixed-conifer forest PLoS One 2012 7 httpsdoiorg101371journalpone0036131 PMID

22567132

37 Blundell AG Peart DR Density-dependent population dynamics of a dominant rain forest canopy tree

Ecology 2004 85 704ndash715

38 Bagchi R Swinfield T Gallery RE Lewis OT Gripenberg S Narayan L et al Testing the Janzen-Con-

nell mechanism Pathogens cause overcompensating density dependence in a tropical tree Ecol Lett

2010 13 1262ndash1269 httpsdoiorg101111j1461-0248201001520x PMID 20718845

39 Inman-Narahari F Ostertag R Hubbell SP Giap NX Cordell S Sack L Density-dependent seedling

mortality varies with light availability and species abundance in wet and dry Hawaiian forests J Ecol

2016 104 773ndash780 httpsdoiorg1011111365-274512553

40 Wright SJ Plant diversity in tropical forests A review of mechanisms of species coexistence Oecolo-

gia 2002 130 1ndash14 httpsdoiorg101007s004420100809 PMID 28547014

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41 Schnitzer SA Klironomos JN HilleRisLambers J Kinkel LL Reich PB Xiao K et al Soil microbes

drive the classic plant diversityndashproductivity pattern Ecology 2011 92 296ndash303

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2016

43 Appanah S Turnbull JM editors A review of Dipterocarps Taxonomy Ecology and Silviculture

Bogor Indonesia Center for International Forestry Reseach 1998

44 Brearley FQ Banin LF Saner P The ecology of the Asian dipterocarps Plant Ecol Divers 2016 9

429ndash436 httpsdoiorg1010801755087420171285363

45 Sapkota IP Oden PC Gap characteristics and their effects on regeneration dominance and early

growth of woody species J Plant Ecol 2009 2 21ndash29 httpsdoiorg101093jpertp004

46 Born J Bagchi R Burslem DFRP Nilus R Tellenbach C Pluess AR et al Differential responses of

dipterocarp seedlings to soil moisture and microtopography Biotropica 2015 47 49ndash58 httpsdoi

org101111btp12180

47 Tito de Morais C Ghazoul J Maycock CR Bagchi R Burslem DFRP Khoo E et al Understanding

local patterns of genetic diversity in dipterocarps using a multi-site multi-species approach Implica-

tions for forest management and restoration For Ecol Manage 2015 356 153ndash165 httpsdoiorg

101016jforeco201507023

48 Ashton PMS Gunatilleke CVS Seedling survival and growth of four Shorea species in a Sri Lankan

rainforest J Trop Ecol 1995 11 263ndash279 httpsdoiorg101017S0266467400008737

49 Paine CET Stenflo M Philipson CD Saner P Bagchi R Ong RC et al Differential growth responses

in seedlings of ten species of Dipterocarpaceae to experimental shading and defoliation J Trop Ecol

2012 28 377ndash384 httpsdoiorg101017S0266467412000326

50 Ashton MS Gunatilleke CV Singhakumara BM Gunatilleke IAUN Restoration pathways for rain for-

est in southwest Sri Lanka a review of concepts and models For Ecol Manage 2001 154 409ndash430

httpsdoiorg101016S0378-1127(01)00512-6

51 Bischoff W Newbery DM Lingenfelder M Schnaeckel R Petol GH Madani L et al Secondary suc-

cession and dipterocarp recruitment in Bornean rain forest after logging For Ecol Manage 2005 218

174ndash192 httpsdoiorg101016jforeco200507009

52 Kettle CJ Ecological considerations for using dipterocarps for restoration of lowland rainforest in

Southeast Asia Biodivers Conserv 2010 19 1137ndash1151 httpsdoiorg101007s10531-009-

9772-6

53 Phan KL Newman M Khou E Hoang VS Vu VD Nguyen HN et al Dipterocarpus dyeri In The

IUCN Red List of Threatened Species 2017 eT33011A2830391 [Internet] 2017 [cited 26 Feb 2017]

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Publishing House 2005

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httpsdoiorg101600036364404772974374

56 Michon G de Foresta H Kusworo Levang P The Damar Agroforests of Krui Indonesia Justice for

Forest Farmers In Zerner C editor People Plants and Justice The Politics of Natural Conservation

Columbia University Press 1999 p 159 httpsdoiorg1043249781936331840

57 Budidarsono S Arifatmi B de Foresta H Tomich TP Damar Agroforest Establishment and Sources of

Livelihood A profitablility assessment of damer agroforest system in Krui Lampung Sumatra Indone-

sia Int Cent Res Agroforesty Bogor Indonesia 2000

58 Hai Ha NT Duc NM Hien DP Duy VD Don PQ Tuan Anh N Le et al Genetic diversity of Dipterocar-

pus dyeri in the tropical forests of Tan Phu (Dong Nai) TAP CHI SINH HOC 2016 38 81ndash88 https

doiorg10156250866-7160v38n17531

59 Shugart HH A Theory of Forest Dynamics The Ecological Implications of Forest Succession Models

New York Berlin Heildelberg Tokyo Springer-Verlag 1984

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tional 1994

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aboutterms-of-use

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natural-sciencesenvironmentecological-sciencesbiosphere-reservesasia-and-the-pacificvietnam

dong-nai

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khı hậu Việt Nam Ha Noi Ha Noi National University 2000

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PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 17 20

65 Pham QK Nguyen XN Tra NP Nguyen VK Hua AT Le AT Soil map of Dong Nai Province Ho Chi

Minh City Vietnam MARD 2004

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tion system for naming soils and creating legends for soil maps Rome FAO 2014

67 Blanc L Maury-Lechon G Pascal J-P Structure floristic composition and natural regeneration in the

forests of Cat Tien National Park Vietnam an analysis of the successional trends J Biogeogr 2000

27 141ndash157 httpsdoiorg101046j1365-2699200000347x

68 Thai VT Những hệ sinh thai rừng nhiệt đới Việt Nam [Tropical forest ecosystems in Vietnam] Ho Chi

Minh City Vietnam Nhagrave xuất bản Khoa học vagrave Kỹ Thuật [Science and Technics Publishing House]

1999

69 Thai VT Phat sinh quần thể vagrave phan loại thảm thực vật nhiệt đới ở Việt Nam [Eco-genesis and classifi-

cation of forest vegetation of Vietnam (From ecosystem perspective)] First HagraveNội Vietnam Science

and Techniques Publishing House 1963

70 McElwee PD Forests Are Gold Trees People and Environmental Rule in Vietnam University of

Washington Press 2016

71 Millet J Pascal JPP Kiet LCC Effects of disturbance over 60 years on a lowland forest in southern

vietnam J Trop For Sci 2010 22 237ndash246 Available httpwwwtandfonlinecomdoiabs101198

016214504000001303

72 Williams LJ Bunyavejchewin S Baker PJ Deciduousness in a seasonal tropical forest in western

Thailand interannual and intraspecific variation in timing duration and environmental cues Oecolo-

gia 2008 155 571ndash582

73 Frazer GW Canham CD Lertzman KP Gap Light Analyzer (GLA) Imaging software to extract can-

opy structure and gap light transmission indices from true-colour fisheye photographs users manual

and program documentation Simon Fraser University Burnaby British Columbia and the Institute of

Ecosystem Studies Millbrook New York 1999

74 Nobis M SideLook 11mdashImaging software for the analysis of vegetation structure with true-colour pho-

tographs 2005

75 Nobis M Hunziker U Automatic thresholding for hemispherical canopy-photographs based on edge

detection Agric For Meteorol 2005 128 243ndash250 httpsdoiorg101016jagrformet200410002

76 Beven KJ Kirkby MJ A physically based variable contributing area model of basin hydrology Hydrol

Sci Bull 1979 24 43ndash69 httpsdoiorg10108002626667909491834

77 Raduła MW Szymura TH Szymura M Topographic wetness index explains soil moisture better than

bioindication with Ellenbergrsquos indicator values Ecol Indic 2018 85 172ndash179 httpsdoiorg101016

jecolind201710011

78 Soslashrensen R Zinko U Seibert J On the calculation of the topographic wetness index Evaluation of dif-

ferent methods based on field observations Hydrol Earth Syst Sci 2006 10 101ndash112 httpsdoiorg

105194hess-10-101-2006

79 R Development Core Team R A language and environment for statistical computing Vienna Austria

R Foundation for Statistical Computing 2018 httpswwwr-projectorg

80 Wang Y Naumann U Wright ST Warton DI Mvabund- an R package for model-based analysis of

multivariate abundance data Methods Ecol Evol 2012 3 471ndash474 httpsdoiorg101111j2041-

210X201200190x

81 Wang Y Naumann U Eddelbuettel D Warton D Byrnes J Silva R dos S et al mvabund Statistical

Methods for Analysing Multivariate Abundance Data 2018 httpscranr-projectorgpackage=

mvabund

82 Venables WN Ripley BD Modern Applied Statistics with S Fourth New York Springer 2002

83 Bates D Machler M Bolker B Walker S Fitting Linear Mixed-Effects Models using lme4 J Stat Softw

2015 67 1ndash48 httpsdoiorg1018637jssv067i01

84 Baringaringth R Bayesian First Aid tba 2013 tba

85 Kenzo T Yoneda R Matsumoto Y Azani MA Majid NM Leaf photosynthetic and growth responses

on four tropical tree species to different light conditions in degraded tropical secondary forest Peninsu-

lar Malaysia Jarq-Japan Agric Res Q 2008 42 299ndash306

86 Baskin CC Baskin JM Seed dormancy in trees of climax tropical vegetation types Trop Ecol 2005

46 17ndash28

87 OrsquoBrien MJ Philipson CD Tay J Hector A The Influence of variable rainfall frequency on germination

and early growth of shade-tolerant dipterocarp seedlings in Borneo PLoS One 2013 8 1ndash9 https

doiorg101371journalpone0070287 PMID 23894634

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 18 20

88 Zipperlen SW Press MC Photosynthesis in relation to growth and seedling ecology of two dipterocarp

rain forest tree species J Ecol 1996 84 863ndash876 httpsdoiorg1023072960558

89 Cao K Booth EW Leaf anatomical structure and photosynthetic induction for seedlings of five diptero-

carp species under contrasting light conditions in a Bornean heath forest J Trop Ecol 2001 17 163ndash

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90 Chua SC Potts MD The role of plant functional traits in understanding forest recovery in wet tropical

secondary forests Sci Total Environ 2018 642 1252ndash1262 httpsdoiorg101016jscitotenv2018

05397 PMID 30045506

91 Ashton MS Gunatilleke CVS Gunatilleke IAUN Singhakumara BMP Gamage S Shibayama T et al

Restoration of rain forest beneath pine plantations A relay floristic model with special application to

tropical South Asia For Ecol Manage 2014 329 351ndash359 httpsdoiorg101016jforeco201402

043

92 Griscom HP Ashton MS Restoration of dry tropical forests in Central America A review of pattern

and process For Ecol Manage 2011 261 1564ndash1579 httpsdoiorg101016jforeco201008027

93 Ashton PMS Goodale UM Bawa KS Ashton PS David Neidel J Restoring working forests in human

dominated landscapes of tropical South Asia An introduction For Ecol Manage 2014 329 335ndash339

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94 Paoli GDD Curran LMM Zak DRR Soil nutrients and beta diversity in the Bornean Dipterocarpaceae

evidence for niche partitioning by tropical rain forest trees J Ecol 2006 94 157ndash170 httpsdoiorg

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95 Whitmore TC Brown ND Dipterocarp seedling growth in rain forest canopy gaps during six and a half

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19960102

96 Itoh A Yamakura T Ogino K Lee HS Survivorship and growth of seedlings of four dipterocarp spe-

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openness on the regeneration of Dipterocarpus turbinatus CF Gaertn (Dipterocarpaceae) in a pro-

tected forest area of Bangladesh Trop Ecol 2016 57 455ndash464

98 Weiskittel AR Hann DW Kershaw JA Vanclay JK Forest Growth and Yield Modeling Chichester

UK John Wiley amp Sons Ltd 2011 httpsdoiorg1010029781119998518

99 Chong KY Chong R Tan LWA Yee ATK Chua MAH Wong KM et al Seed production and survival

of four dipterocarp species in degraded forests in Singapore Plant Ecol Divers 2016 9 483ndash490

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100 Bagchi R Henrys PA Brown PE Burslem DFRP Diggle PJ Gunatilleke CVS et al Spatial patterns

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101 Bagchi R Press MC Scholes JD Evolutionary history and distance dependence control survival of

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PMID 19849708

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104 Mangan SA Schnitzer SA Herre EA MacK KML Valencia MC Sanchez EI et al Negative plant-soil

feedback predicts tree-species relative abundance in a tropical forest Nature 2010 466 752ndash755

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105 Schnitzer SA Carson WP Treefall gaps and the maintenance of species diversity in a tropical forest

Ecology 2001 82 913ndash919

106 Oshima C Tokumoto Y Nakagawa M Biotic and abiotic drivers of dipterocarp seedling survival follow-

ing mast fruiting in Malaysian Borneo J Trop Ecol 2015 31 129ndash137 httpsdoiorg101017

S026646741400073X

107 Lebrija-Trejos E Reich PB Hernandez A Wright SJ Species with greater seed mass are more toler-

ant of conspecific neighbours a key driver of early survival and future abundances in a tropical forest

Ecol Lett 2016 19 1071ndash1080 httpsdoiorg101111ele12643 PMID 27346439

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vagrave sự biến đổi cấu truc gen protein của một số loagravei sinh vật tại khu vực MatildeĐagrave Minist Sicence Tech-

nol HagraveNội Viet Nam Bộ Khoa học vagraveCong Nghệ (Ministry of Science and Technology) 2010

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 19 20

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lishment and growth Their role for distribution of tree species across a tropical rainfall gradient PLoS

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Using Caribbean Pine Pinus caribaea as a Nurse for Establishing Late-Successional Tree Species J

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113 Ito S Mizoue N Kajisa T Heng Sokh VM Hirata R Mitsuda Y Analysis of growth traits of Hopea reco-

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2010

114 Deb JC Phinn S Butt N McAlpine CA The impact of climate change on the distribution of two threat-

ened Dipterocarp trees Ecol Evol 2017 7 2238ndash2248 httpsdoiorg101002ece32846 PMID

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115 Cao K Water relations and gas exchange of tropical saplings during a prolonged drought in a Bornean

heath forest with reference to root architecture J Trop Ecol 2000 16 S0266467400001292 https

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cbo9781107323506013

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forest Oecologia 2011 165 161ndash168 httpsdoiorg101007s00442-010-1707-0 PMID 20607296

PLOS ONE Climax species recruitment in secondary forest

PLOS ONE | httpsdoiorg101371journalpone0233524 May 29 2020 20 20